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Two Cases of Severe Obstructive Pneumonia Associated with an Hku1-Like Coronavirus

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Two Cases of Severe Obstructive Pneumonia Associated with an Hku1-Like Coronavirus 134 EU RO PE AN JOUR NAL OF MED I CAL RE SEARCH March 26, 2007 Eur J Med Res (2007) 12: 134-138 © I. Holzapfel Publishers 2007 TWO CASES OF SEVERE OBSTRUCTIVE PNEUMONIA ASSOCIATED WITH AN HKU1-LIKE CORONAVIRUS B. Kupfer2*, A. Simon1*, C. M. Jonassen4, S. Viazov3, V. Ditt3, R.-L. Tillmann2, A. Müller1, B. Matz2, O. Schildgen2 1Department of Pediatrics, 2Institute for Medical Microbiology, Immunology, and Parasitology, University of Bonn, 3Institute for Virology, Essen University Hospital, 4National Veterinary Institute, Norway Abstract these pathogens could lead to mild to severe respirato- Background: During the last few years a number of ry tract infections (RTI) within all age groups. Despite previously undescribed viruses, including human some reports from different parts of the world have metapneumovirus, coronaviruses SARS, NL63 and described the occurrence of HKU1 coronavirus (Es- HKU1, and bocavirus, were identified in nasopharyn- per et al. 2006; Sloots et al. 2006; Vabret et al. 2006), geal samples from patients with signs of respiratory there is still little information about the virus, its dis- infections. These viruses may cause mild to life-threat- tribution, and its phylogeny. Here we describe the de- ening infections. tection of RNA from a new variant of HKU1 coron- Objectives: Nasopharyngeal samples from hospitalized avirus in two children hospitalized with respiratory pediatric patients with respiratory disease were tract infections in Germany. analysed for the presence of coronaviruses and other well known and newly identified respiratory viruses. PATIENTS AND METHODS Results: Two clinical cases of a severe obstructive pneumonia, which were associated with the presence CLINICAL SAMPLES AND PCR of RNA of a novel variant (subtype) of HKU1 coron- Nasopharyngeal aspirates were collected from hospi- avirus in the nasopharyngeal aspirates, were identified. talized pediatric patients between October 2003 and Discussion: The detection of a HKU1-like coronavirus May 2006 in the Department of Pediatrics of the Uni- in pediatric patients in the current study complement versity Hospital in Bonn, Germany. A total number of the most recent independent finding of similar or 296 samples were analysed for the presence of human closely related coronaviruses in patients with respira- coronaviruses. tory diseases in France (Vabret et al. 2006) and Nor- Therefore, RNA was extracted from nasopharyn- way (Jonassen et al., see accompanying manuscript). geal aspirates with the RNeasy protect kit (QIAGEN, These observations indicate a wide dissemination of Hilden, Germany) and subjected to a single-step RT- HKU1-like coronaviruses in Europe. PCR (QIAGEN, Hilden, Germany) using a set of primers designed on the basis of comparison of pol INTRODUCTION ORF1b sequences of known human coronaviruses. Basically, this approach was a modification of the Beside the commonly known viruses that cause respira- technique described by Stephensen et al. (1999) and tory tract infections in children like respiratory syncytial Moes et al. (2005). RT was carried out for 30 min at virus (RSV), rhinoviruses, adenoviruses, and the human 42°C followed by a PCR with one initial step of Taq- coronaviruses OC43 and 229E, an increasing number Polymerase activation (95 °C for 15 min.), 35 cycles of of respiratory viruses were detected recently. These amplification (95 °C for 30 sec., 50 °C for 30 sec., pathogens include human metapneumovirus (van den 72 °C for 30 sec) and a final elongation step (72 °C for Hoogen et al. 2001), human bocavirus (Allander et al. 5 min). The primers used for the pan-coronavirus 2005) and three different coronaviruses. In 2003 one PCR were sv387as (5’ – TCA CAY TTW GGA TAR single outbreak of the SARS coronavirus evolved to a TCC CA), sv388s (5’ – ACT CAR ATR AAT CTT worldwide problem with high mortality rates of the in- AAR TAY GC), and sv389s (5’ – ACT CAA ATR fected patients (Drosten et al. 2003). Two other coron- AAT TTR AAR TAY GC) at final concentrations of aviruses, namely the human coronavirus NL-63 (van 0.6µM each. PCR-amplicons with a length of 251 der Hoek et al, 2004) also known as coronavirus NL basepairs were electrophoresed on an agarose gel and (Fouchier et al. 2004) and the human coronavirus visualized by ethidium bromide staining. HKU1 (Woo et al. 2005) have been identified recently. Samples were also screened for the presence of hu- The coronaviruses NL63 and HKU1 seem to be man metapneumovirus (HMPV) (Viazov et al. 2003; distributed worldwide and in contrast to SARS coron- Schildgen et al. 2004), RSV (Kupfer et al. 2006; Müller avirus, they occur more frequently. Infections with et al., submitted; Wilkesmann et al. 2006), influenza viruses A and B (Müller et al., submitted for publica- tion; Wilkesmann et al. 2006), and bocavirus (Allander * The first two authors contributed equally to this paper. et al. 2005). March 26, 2007 EUROPEAN JOURNAL OF MEDICAL RESEARCH 135 SEQUENCING OF CORONAVIRAL PCR-AMPLICONS AND of an atypical pneumonia. His clinical picture was PHYLOGENETIC ANALYSIS characterized by a severe obstructive bronchitis, cough, wheezing, and tachypnoea (52 per minute). Amplicons were purified using the QIAquick PCR pu- Compared to patient 1 the clinical symptoms were less rification kit (Qiagen, Hilden, Germany) and subjected severe (no supplemental oxygen required), but severe to sequencing in both directions (BigDye Terminator enough to require a 7 days stay in hospital. At admis- DNA sequencing kit, Applied Biosystems, Darmstadt, sion the body temperature (36.9°C) was normal and Germany) as previously described (Schildgen et al. because of the severe respiratory symptoms he re- 2004). BlastN (http://www.ncbi.nlm.nih.gov/BLAST) ceived beta-mimetics, ipratropium bromide for 3 days, was used for comparison of the obtained sequences to and intravenous antibiotics for 4 days, despite the ab- nucleotide sequence databases. Viral sequences were sence of signs of an bacterial infection (CRP 3.6 aligned to the corresponding sequences of coron- mg/l, leukocyte count 6300/µl). avirus HKU1 (accession number: AY597011), SARS In nasopharyngeal washes from both patients, RNA coronavirus (AY515512), coronavirus OC43 from a novel HKU1-like coronavirus could be identi- (AY585229), coronavirus NL63 (AY567487), and a fied by RT-PCR. very recently described coronavirus strain (NO/0053/04; AM261821) using ClustalX version 1.8 PHYLOGENETIC ANALYSIS (Thompson et al. 1997). Phylogenetic trees of the newly derived sequences The nucleic acid sequences obtained from the direct were constructed by the neighbour-joining method sequencing of the coronavirus amplificons were ini- (Saitou & Nei, 1987). Reliability of the topology of tially submitted to a nucleotide-nucleotide blast the tree was evaluated by the bootstrap resampling (BlastN). This analysis revealed a similarity of 92% to method using 1000 replicates. The generated tree was the HKU1 group of coronaviruses. Most surprisingly, visualized with the program NJplot (Perrière et al. an exact match (100% identity) (Fig. 1A), and 99,5% 1996). identity, were found to coronaviruses NO/0053/04 and NO/0341/04, respectively, identified in Norway RESULTS from infants presenting respiratory tract infections in winter 2004/5 (Jonassen et al., submitted). Phyloge- In the present study 296 nasopharyngeal samples from netic analysis of the identified viruses (DE/0411 and hospitalized pediatric patients suffering from respira- DE/0415) from both patients together with tory symptoms were analysed by RT-PCR for coron- NO/0053/04 sequence revealed a novel coronavirus aviruses. As controls, specimens from 15 healthy adult variant within the HKU1 cluster (Fig. 2). However, no volunteers were tested. differences between HKU1, DE/0411 and DE/0415 The most frequent pathogens detected were human were observed on the amino acid level (Fig. 1B). Of paramyxoviruses RSV and HMPV (manuscript in note, within the analysed amino acid sequence in this preparation). Coronaviruses were detected in five cas- portion of the viral replicase gene, there is only one es (1.7%). In three out of the five episodes of coron- substitution between HKU1 and OC43 (Fig. 1B). Phy- avirus-associated respiratory disease, the well charac- logenetic analysis showed higher divergence of the terized human coronavirus OC43 was identified by se- HKU1-like variants to the human pathogenic SARS quence analysis. Surprisingly, sequence analysis of coronavirus (branching off the root of the group II coronavirus PCR amplicons derived from the two re- coronaviruses) and coronavirus NL63 (group I coron- maining individuals revealed in both cases a novel avirus) on the nucleotide, as well as on the amino acid coronavirus variant. level (Fig. 1 and Fig. 2). CLINICAL CASES DISCUSSION The first patient with a coronavirus infection was a 16 During the last five years an increasing number of vi- months old boy admitted to the hospital with wheez- ral respiratory pathogens have been newly identified. ing, cough, fever (38.5°C), and a reduced general con- This includes three new coronaviruses, namely the dition. He was hospitalized for 14 days, and due to his SARS coronavirus (Drosten et al. 2003), the human reduced general condition and elevated inflammatory coronavirus NL63 (van der Hoek et al. 2004; Fouchier laboratory markers (CRP level 13.8 mg/L; leukocyte et al. 2004), and the coronavirus HKU1 (Woo et al. count 14.2 x 109/L) he received inhalative treatment 2005). Nevertheless, there is still a certain proportion with beta-mimetics, ipratropium bromide, budesonide of RTIs without an identified pathogen. Some RTIs in (7 days each) in addition with inhalative corticoids for our cohort were associated with human coronaviruses 6 days and systemic steroids for 3 days. No antibiotics but neither the SARS coronavirus nor the human were given since the chest radiography revealed no coronavirus NL63 could be detected in the nasopha- signs of a bacterial pneumonia. The child required ryngeal samples. The first reason for this observation supplemental oxygen for 4 days; the clinical severity is probably that the SARS outbreak was a rather single was 2 on the modified McIntosh scale (Wilkesmann et zoonotic event whereas other coronaviruses circulate al.
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